Elsevier Editorial System(tm) for Journal of Veterinary Behavior: Clinical Applications and Research
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Manuscript Number: JVEB-D-13-00049R2
Title: Effect of the change of social environment on the behavior of a captive brown bear (Ursus arctos)
Article Type: Original Research Paper
Keywords: brown bear; behavior; sleep; animal welfare; zoo Corresponding Author: Prof. Silvana Mattiello, Ph.D.
Corresponding Author's Institution: University of Milan First Author: Silvana Mattiello, Ph.D.
Order of Authors: Silvana Mattiello, Ph.D.; Serena M Brignoli; Antonella Cordedda; Bernardo Pedroni;
Cristina Colombo; Fabia Rosi
Milano, January 7
th, 2014
Dear Editor,
thank you very much for your answer.
I made all the changes required by the reviewer. I hope that the pictures of the enclosure are in line with the reviewer’s request.
I also included all the additional information that you required in your e-mail.
I hope that this new version will be acceptable for publication.
Best regards and Happy New Year!
Silvana Mattiello
Cover Letter
Answers to reviewer’s comments:
1. Lines 84-90
I suggest moving even incomplete results of earlier studies on these two bears to section "Results"
as an "unpublished data". I do not share the opinion that much more additional information would be needed.
Au: I moved this part to the beginning of the Results section.
2. Line 79
(Fig. 1) While suggesting a picture I meant photo rather or schematic drawing. I suggest again as explained, that authors provide a photo or schematic drawing (preferably black and white or grey scale) of the enclosure.
Au: I replaced the map with a photo-collage with views on different parts of the enclosure (and modified the Figure caption accordingly). Sorry if I misunderstood the previous suggestion!
*Detailed Response to Reviewers
1
Effect of the change of social environment on the behavior of a captive brown bear (Ursus 1
arctos) 2
3
Silvana Mattiello1, Serena Maria Brignoli1, Antonella Cordedda1, Bernardo Pedroni2, Cristina 4
Colombo3, Fabia Rosi4 5
6
1Università degli Studi di Milano, Dipartimento di Scienze Veterinarie e Sanità Pubblica 7
2Osservatorio Eco-Faunistico Alpino, Aprica (SO), Italy 8
3Unità Operativa Psichiatria 1 – San Raffaele Turro, Istituto Scientifico Universitario Ospedale San 9
Raffaele, Milano 10
4Università degli Studi di Milano, Dipartimento di Scienze Agrarie e Ambientali - Produzione, 11
Territorio, Agroenergia 12
13 14
Corresponding author: Prof. Silvana Mattiello. Università degli Studi di Milano, Dipartimento di 15
Scienze Veterinarie e Sanità Pubblica, Via Celoria 10, 20133 Milano, Italy - Tel. +39 02 5031 8040 - 16
Fax: +39 02 5031 8030 – E-mail: Silvana.Mattiello@unimi.it 17
18 19 20
*Manuscript
Click here to view linked References
2 Abstract
21
We observed the behavior of a captive sterilized male brown bear before and after the death of his 22
female sibling, in order to investigate the effect of the change of social environment on his behavior 23
and welfare. Observations were carried out by continuous recording during daylight for 6 weeks prior 24
to hibernation when the bear was kept with the sibling, and they were repeated two years later, when 25
the bear was alone (total observation time=108 h).
26
Feeding, moving and the total amount of time spent resting (including sleeping and alert inactive) 27
were not affected by the change of social environment. However, when the bear was alone the 28
percentage of time he spent alert inactive almost trebled (pair: 17.7±3.3, alone: 48.5±5.5; P<0.001) 29
and the time spent sleeping was less than one third (pair: 51.1±6.1, alone: 14.2±5.0; P<0.001) than 30
when the female was present. The bear spent most of his sleeping time in lateral lying posture (a 31
posture probably associated with REM sleep). The percentage of time dedicated to this posture was 32
significantly reduced after the death of his sibling (pair: 35.9%±7.4, alone: 15.0%±5.4; P<0.05), 33
whereas the percentage of time spent in quadrupedal posture increased (pair: 17.1%±5.4, alone:
34
37.8%±7.8; P<0.05). One of the possible reasons for these changes may be an increased risk 35
perception of the bear after the death of his sibling. Our results highlight the importance of social 36
environment and of its changes, which should be carefully considered in order to maintain captive 37
bears in good welfare conditions.
38 39
Keywords: brown bear, behavior, sleep, animal welfare, zoo.
40 41 42
3 Introduction
43
According to the International Species Information System (ISIS), at least 561 brown bears of 44
various subspecies are kept in zoos around the world (as of March 22, 2013), either in group 45
(n=79) or as individual animals (n=482). This raises some welfare issues, as captivity implies a 46
number of environmental and management restrictions that may affect bears’ welfare (Poole, 47
1994; O’Grady, 1994).
48
One of the key issues of bear management in captivity is the social environment. Captivity can 49
induce modifications of social behavior, for example in response to forced aggregations of 50
individuals. Anecdotal information based on sporadic observation in zoos (Poulsen, 2011) 51
report that these forced aggregations can sometimes result in aggressive interactions or, in some 52
cases, they may lead to the establishment of friendly relationships that may last for a lifetime, in 53
spite of the solitary attitude of the species. Bears are usually regarded as solitary animals, with a 54
promiscuous mating system (Schwartz et al., 2003; Bellemain et al., 2006). This means that they 55
can show some sort of social behavior, which varies from strict territoriality to more or less 56
developed forms of social aggregation (Sandell, 1989). This plasticity makes the animals able to 57
adapt to different situations. Bear social attitudes can present some variations in response to 58
several factors, such as individual genetic factors (Stirling and Derocher, 1990) and the season 59
or the environmental conditions in which animals are living. A more or less developed social 60
behavior may depend, for example, from resource distribution: where resources are scarce, 61
bears are likely to be more solitary, whereas in case of high density of high quality food (e.g. in 62
captive environment, where food is always guaranteed) they may show a trend to aggregate with 63
other individuals (Stirling and Derocher, 1990). Other forms of aggregation may be observed 64
for females, which can remain with their cubs, and for littermates, which may continue to 65
associate with one another, playing and feeding together (Novak, 1999). In brown bear this 66
association, based on relatedness, is particularly relevant for females, whereas males tend to 67
disperse far from their relatives (Støen et al., 2005).
68
4
Throughout the year, we can observe different behavioral phases, mainly related to the 69
reproductive cycle, that may modify the social attitudes of bears, leading to a gregarious 70
tendency (Mustoni, 2004).
71
An open issue for discussion on bears’ welfare in captivity is whether males and females should 72
be kept together all year round (Poole, 1994). This is particularly relevant when bears are 73
sexually active and approach the reproductive season. In order to limit stress and to prevent 74
undesired births, some zoos choose to sterilize the animals or vasectomize the males (O’Grady, 75
1994).
76
This study was carried out in order to investigate the effect of the change of social environment 77
on the behavior of a captive sterilized male brown bear, which spent all his life together with his 78
sister, and suddenly remained alone after her death.
79 80
Material and methods 81
The subject of the present study is Orfeo, a male brown bear born in captivity in 1990 and kept 82
since 2007 in an enclosure at the Osservatorio Eco-Faunistico Alpino of the Orobie Valtellinesi 83
Park, a tourist area of natural interest, open to visitors, located in Aprica (Province of Sondrio, 84
Northern Italy), at 1650 m a.s.l..
85
The double fenced enclosure has a surface area of approximately 10,000 m2 and includes 86
meadows, a mixed conifer wooded area, some rocks, a stream, a pond, two artificial dens and 87
two natural dens dug by the bears (Fig. 1). Feed was delivered every morning and consisted of 88
variable proportions of vegetables (e.g. carrots, apples, or fennels), meat or fish, and honey.
89
Until the beginning of 2011, Orfeo had been living together with his twin sister. Both animals 90
had been sterilized, in order to prevent undesired births. The behavior of both bears was 91
observed in 2009 during the pre-hibernation period (end of September - early November;
92
Daldoss, 1981), in order to assess their welfare status in the captive environment.
93
5
Orfeo’s sibling never woke up after the hibernation period of winter 2010-2011. Following her 94
death, in autumn 2011 further observations were carried out on Orfeo alone, implementing the 95
same observation protocol used in 2009, in order to detect possible changes of the bear’s 96
behavior in response to the modification of his social environment. Both in 2009 and in 2011, 97
the protocol consisted of direct continuous recording observations (Martin and Bateson, 1993), 98
conducted during daylight for 6 weeks prior to hibernation. During each week, three observation 99
sessions (3 h each) were carried out: one in the morning (from 9:00 to 12:00), one in the 100
afternoon (from 12:00 to 15:00) and one in the evening (from 15:00 to 18:00). The total 101
observation time was 108 h (3 h x 3 sessions x 6 wk x 2 y).
102
Orfeo was observed from a high platform (an observation terrace normally used also by the 103
visitors of the Osservatorio) with the aid of an 8 x 30 magnification binoculars.
104
The following behavioral categories were recorded: feeding (eating or chewing food, either 105
delivered by the keeper or found in the fence, e.g. leaves or branches); drinking; moving 106
(walking or hurrying, including movement while sniffing or foraging); sleeping (a state of 107
behavioral quiescence, the body is completely relaxed, the eyes are closed and the bear is not 108
reactive to any external stimulus); alert inactive (the bear is not moving, but his eyes are open 109
and he is reactive to external stimuli); den preparation (including digging and raking or mowing 110
vegetable parts to prepare for hibernation); self-grooming (including self-licking, self- 111
scratching, scratching against trunks or rocks, bathing and scrolling) and stereotypies (pacing, 112
circling or walking in figure-of-eight, head-tossing, swaying; Montaudouin and Le Pape, 2005).
113
All behavioral categories were mutually exclusive. Additionally, the following postures were 114
also recorded: quadrupedal posture (standing or moving on the 4 legs); lateral lying (the bear is 115
lying on a side, with outstretched legs and neck, occasionally with one leg partially bent);
116
sterno-costal lying (the weight of the bear is loaded on the ventral part of the body, the fore legs 117
are outstretched, while the hind legs are bent below the body, the head is usually upright, 118
6
occasionally outstretched) and sitting (the bear is sitting on his hindquarters, leaning on the 119
distal portion of his front legs, like a dog) (Fig. 2). All postures were mutually exclusive.
120
Orfeo was visible for most of the time, except when he was in the den or obscured by trees. The 121
duration of each activity/posture was expressed in minutes; the percentage of time dedicated to 122
each activity/posture out of the total visible observation time was then calculated. These 123
variables were submitted to non-parametric analysis of variance (Mann-Whitney test; SPSS, 124
2007), in order to test the effect of social environment (in pair vs alone) on the behavior of the 125
brown bear. Results are presented as means ± standard errors of the percentage of time 126
dedicated to each behavioral category and to each posture. Preliminary analysis showed a very 127
similar trend of behavioral rhythms for both years, therefore the results regarding the effect of 128
time band (morning, afternoon, evening) will not be reported.
129 130
Results 131
The observations carried out on the pair in 2009 showed that bears exhibited a wide range of 132
behaviors, reflecting their ethogram in the wild (with peaks of feeding activity in the morning, 133
and peaks of resting activity in the middle of the day), and that they were free from stereotypies 134
or other abnormal behaviors. These findings suggested that the enclosure where they lived, and 135
the management practices to which they were submitted, were adequate to guarantee their 136
welfare in the captive environment (unpublished data).
137
Behavioral categories 138
During the total observation period (2009 and 2011), Orfeo spent the majority of his time alert 139
inactive (33.1%), followed by sleeping (32.7%), feeding (16.1%) and moving (9.5%). The rest 140
of the time was dedicated to self-grooming (4.4%), den preparation (4.1%) and drinking (0.1%).
141
No stereotypies were ever recorded. Behavioral categories with low or null occurrence were not 142
statistically analyzed.
143
7
Feeding and moving time were not affected by the change of the social environment. The total 144
amount of time spent resting (including sleeping and alert inactive) was also very similar in both 145
periods (68.7%±4.7 in pair vs 62.7%±5.3 alone). However, the proportion of time sleeping and 146
alert inactive was reversed: when Orfeo was alone, the time he spent alert inactive almost 147
trebled and the time spent sleeping was less than one third than when his sibling was present 148
(Fig. 2). These differences were statistically significant (P<0.001 for both behavioral 149
categories).
150 151
Postures 152
Orfeo spent 39.2% of his time in lateral lying posture, 27.4% of his time in quadrupedal posture, 153
25.5% sterno-costal lying and 7.9% sitting.
154
When he was alone, Orfeo spent significantly less time in lateral lying and more time in 155
quadrupedal posture than when he was in pair (Fig. 3; P<0.05 for both postures), while the time 156
spent sitting and in sterno-costal lying was not affected by the change of the social environment.
157
The time allocated to different behavioral categories during each posture is reported in Tab. 1.
158
Orfeo spent most of his sleeping time in lateral lying posture. When he was sitting or in sterno- 159
costal lying posture, he spent most of the time inactive but vigilant (alert inactive). Feeding was 160
performed during sterno-costal lying or quadrupedal posture. Moving and den preparation were 161
performed almost exclusively in quadrupedal posture.
162 163
Discussion 164
Orfeo spent a high overall proportion of time resting, either sleeping or alert inactive. This is in 165
agreement with observations on wild bears, which use most of daylight time for resting, while 166
their activity is mainly concentrated during the evening and the night (Roth, 1983). However, 167
the resting behavior of the observed brown bear was significantly affected by the change of 168
social environment. The absence of his sibling, which used to be vigilant by Orfeo when he was 169
8
resting (Cordedda, 2010), seems to have induced a reduction of the time dedicated to totally 170
relaxed inactivity, suggesting that Orfeo was in quieter conditions when his sibling was present.
171
The behavior that we described as sleeping (behavioral quiescence, with the body completely 172
relaxed, the eyes closed and no reaction to external stimuli) is very similar to the behavioral 173
phenotype of sleep described by Lima et al. (2005). However, in absence of physiological 174
measures, we cannot state that Orfeo was really sleeping when he was lying inactive and, above 175
all, we cannot distinguish in which phase of sleep (REM (Rapid Eyes Movement) or non REM) 176
he was. This behavior was performed by Orfeo mainly during the lateral lying posture, that 177
seems to be associated to REM sleep in some mammal species, such as cattle (de Wilt, 1985).
178
The fact that most of the time that Orfeo spent in lateral lying posture was dedicated to total 179
inactivity seems to support this statement also for bears. During sleep, and especially during the 180
REM phase, the arousal thresholds tend to be higher than in other states, and therefore animals 181
exposed to predation risk are likely to spend less time sleeping and less time in REM sleep, due 182
to increased vulnerability (Lima et al., 2005). Sleep is a plastic behavior that may dynamically 183
adapt to different environmental situations (Lima et al., 2005). Modifications of social activities, 184
as well as of other factors, such as for example time of light exposure or food availability, can 185
modify the sleep-wake cycle and the SWS-REM cycle (Pitrosky et al., 2003). In many 186
gregarious species, the presence of conspecifics provides a sense of protection to other 187
individuals, whereas isolated animals usually show higher levels of attentiveness, which are 188
probably related to a higher sense of fear of external stimuli (Krebs and Davis, 1993). In fact, 189
animals in risky situations prefer to form groups when they sleep (Krause and Ruxton, 2002).
190
Although bears are usually regarded as predators, and not as prey, a solitary situation may be 191
dangerous for them too, as some risks may occur, such as hunting, and the need for protection is 192
important. In the specific case of bears, the cubs may decide to remain together with their 193
brothers and sisters or to group with other young adults (Novak, 1999), in order to feel more 194
protected. Our results seem to confirm the presence of a similar behavior also in captive brown 195
9
bear and highlight the importance of providing a sense of security for the animals in captivity, 196
as recommended by Poole (1994). Therefore, in our study we can infer that the modification of 197
the social environment can be responsible for the reduction of the time spent sleeping and of the 198
time spent in lateral lying posture, which is strictly associated with a state of total inactivity.
199
Sleep plays a vital role in determining balance among recovery from prior wakefulness and 200
preparation for ensuing wakefulness. Severe sleep disruption, with alteration of the normal 201
restorative functions linked to correct non REM-REM pattern, may alter breathing and 202
cardiovascular functions, and may give rise to impaired emotional reactivity and impairment in 203
cognitive functions (Zepelin and Rechtschaffen, 1974). Furthermore, studies on laboratory 204
rodents demonstrated that REM sleep deprivation represents a stress, which can lead to 205
hyperphagia and increased cardiovascular disease risk (Shaw et al., 1998). Therefore, we may 206
assume that the decrease of time dedicated to the lateral lying posture, possibly related to REM 207
sleep, is connected to a reduced welfare condition. However, in our case Orfeo still seems to be 208
able to cope with the surrounding environment, as his general health status is good, his feeding 209
behavior is normal and he shows no sign of stereotypies.
210
In spite of their solitary attitude, bears can show a strong attachment to other conspecifics, 211
especially if they have been living with them for all their life, as in the case of Orfeo and his 212
sister. Poulsen (2011) reports the case of a female polar bear in captivity that, for the first time 213
in her life, found herself alone and then started to look for a social contact with the zookeeper:
214
although this is an isolated case report, it supports our hypothesis that the break of a social 215
relationship can affect bears’ behavior and that a condition of isolation is not suitable for the 216
welfare of bears that were accustomed to the presence of other conspecifics. In our case, Orfeo 217
was probably habituated to his sister’s presence and had developed a strong bond with her.
218
After the death of his sibling, Orfeo appears in a condition of mental discomfort. This negative 219
condition may be a further cause of the reduction of sleep, as there are growing clinical 220
10
evidences in humans supporting the relationship between depression and sleep disruption 221
(Benedetti and Colombo, 2011).
222 223
Conclusions 224
Our results provide important information for captive bear management. We provide evidence 225
that the change of social environment, and specifically the loss of a conspecific and the 226
subsequent state of isolation and insecurity, may have short-term negative effects on the welfare 227
of captive bears, as the change of activity patterns and the alteration of sleep may interfere with 228
the normal restorative functions of REM sleep. We are uncertain whether these effects will last 229
in the long-term, but preliminary observations suggest that the bear is restoring his normal 230
behavioral patterns. Further research will be carried out in order to confirm these hypotheses.
231
Before the death of Orfeo’s sibling, the pair never showed behavioral problems, suggesting that 232
sterilized males and females can live together in captivity, provided that they have enough 233
resources in their enclosure. The Osservatorio is presently considering the possibility of 234
introducing a new bear mate; however, the risk of aggressive interactions between two 235
unfamiliar adult bears in a confined enclosure is high, and the partition of the existing enclosure 236
is under evaluation, in order to allow a period of acclimation in neighbouring enclosures, that 237
should minimize these risks.
238
Although forcedly based only on one case report, the results of the present study provide new 239
information that open new insights on a previously unexplored field, and highlight the 240
importance of social environment and of its changes, that should be carefully considered in 241
order to maintain good welfare conditions of bears kept in zoos or in other captive 242
environments.
243 244
Acknowledgements 245
11
We are grateful to the Osservatorio Eco-Faunistico Alpino (Aprica) for granting us the access to 246
the bear facilities for behavioral observations. Many thanks to the International Species 247
Information System (ISIS) for providing updated information on brown bear numbers in ISIS 248
member institutions around the world. Finally yet importantly, we acknowledge Leigh Murray 249
for the revision of the English manuscript and an anonymous reviewer for the useful comments 250
on the first version of this manuscript.
251 252
The authors declare no conflict of interest.
253
The idea for the paper was conceived by Bernardo Pedroni and Fabia Rosi.
254
The experiment was designed by Silvana Mattiello.
255
The experiment was performed by Antonella Cordedda and Serena Brignoli.
256
The data were analyzed by Silvana Mattiello.
257
The paper was written by Silvana Mattiello, with help and inputs from all co-authors.
258
No specific funding was provided for this research.
259
The study met all humane standards, as no manipulation was necessary and only non invasive 260
observations were carried out on the subjects.
261 262
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Table 1. Overall percentage of time allocated to different behavioral categories during each 321
posture. Considered behavioral categories are: alert inactive (the bear is not moving, but his 322
eyes are open and he is reactive to external stimuli); sleeping (a state of behavioral quiescence, 323
the body is completely relaxed, the eyes are closed and the bear is not reactive to any external 324
stimulus); feeding (eating or chewing food, either delivered by the keeper or found in the fence, 325
e.g. leaves or branches); moving (walking or hurrying, including movement while sniffing or 326
foraging); self-grooming (including self-licking, self-scratching, scratching against trunks or 327
rocks, bathing and scrolling); den preparation (including digging and raking or mowing 328
vegetable parts to prepare for hibernation); drinking.
329
Observed postures are: quadrupedal posture (standing or moving on the 4 legs); lateral lying 330
(the bear is lying on a side, with outstretched legs and neck, occasionally with one leg partially 331
bent); sterno-costal lying (the weight of the bear is loaded on the ventral part of the body, the 332
fore legs are outstretched, while the hind legs are bent below the body, the head is usually 333
upright, occasionally outstretched); sitting (the bear is sitting on his buttocks, leaning on the 334
distal portion of his front legs, like a dog).
335 336
alert
inactive sleeping feeding moving self- grooming
den
preparation drinking
lateral lying 22.2% 77.6% 0% 0% 0.2% 0% 0%
sterno-costal
lying 75.8% 13.8% 4.6% 0% 5.4% 0.2% 0.2%
quadrupedal
posture 39.8% 0.3% 7.2% 28.6% 3.3% 20.6% 0.2%
sitting 85.6% 0% 0% 0% 12.9% 0% 1.4%
337 338
15 Figure legends
339
Figure 1. Views of the enclosure. a) meadows and mixed conifer wood (the fence can be seen 340
on the right); b) high platform from which the observations were carried out; c) artificial dens;
341
d) natural dens dug by the bears; e) stream.
342 343
Figure 2. Percentage of time (mean ± s.e.) devoted by Orfeo to the main behavioral categories in 344
the presence of his sibling (pair) and alone. Asterisks over the columns indicate significant 345
differences (P<0.001).
346 347
Figure 3. Percentage of time (mean ± s.e.) spent by Orfeo in different postures in the presence of 348
his sibling (pair) and alone. Asterisks over the columns indicate significant differences 349
(P<0.05).
350
Figure 1
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Figure 2
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Figure 3
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